Background adaptation and synapse plasticity in the pars intermedia of Xenopus laevis

Abstract

The amphibian Xenopus laevis adapts the colour of its skin to the colour of its background, by the release of the pro-opiomelanocortin-derived peptide alpha-melanophore-stimulating hormone from the pars intermedia of the pituitary gland. Suprachiasmatic neurons play an important role in adaptation to a light background as they produce the neurotransmitters GABA, dopamine and neuropeptide Y, which inhibit the release of alpha-melanophore-stimulating hormone. These factors are transported to axon varicosities contacting the melanotrope cells. In these varicosities GABA resides in electron-lucent vesicles and neuropeptide Y and dopamine coexist in electron-dense vesicles. In this study the effects of background adaptation on the morphology of the varicosities in the pars intermedia were studied, using immunoelectron microscopy and morphometry with freeze-substitution-fixed material. Varicosities were found singly and in clusters throughout the pars intermedia. Varicosities were identified by the presence of electron-dense and electron-lucent secretory vesicles, the latter being immunopositive for anti-GABA. Both varicosity types revealed active zones with exclusively GABA-containing vesicles in contact with the presynaptic membrane. When white- and black-adapted animals were compared, significant background effects were found with respect to the organization of the varicosities: the density of varicosity profiles was twice as high in white-adapted animals as in black-adapted ones, due to an increase in density of the clustered varicosities. Furthermore, in white-adapted animals varicosities were about twice as large as in black-adapted animals. With respect to vesicle types, single and clustered varicosities showed a differential effect. For both the population of electron-lucent and electron-dense vesicles, single varicosities showed equal numbers in white- and black-adapted animals, but clustered varicosities showed higher numbers of electron-lucent and electron-dense vesicles in black-adapted animals, indicating storage of neurotransmitters. Finally, in varicosities of white-adapted animals the number and size of the active zones and the number of electron-lucent vesicles attached to the active zones, were about twice as high as in black-adapted animals, indicating a stronger GABA release. It is concluded that the profound effects of environmental light conditions on synaptic structure and substructure in the Xenopus pars intermedia are related to a changed release activity of neurotransmitters inhibiting the activity of the melanotrope cells.